Integrated transcriptomic and pathway analyses of sorghum plants revealed the molecular mechanisms of host defense against aphids

Authors: SHRESTHA, KUMAR - Oklahoma State University; HUANG, JIAN - Oklahoma State University; YAN, LIULING - Oklahoma State University; DOUST, ANDREW - Oklahoma State University; Huang, Yinghua

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/3/2024
Publication Date: 6/6/2024
Citation: Shrestha, K., Huang, J., Yan, L., Doust, A., Huang, Y. 2024. Integrated transcriptomic and pathway analyses of sorghum plants revealed the molecular mechanisms of host defense against aphids. Frontiers in Plant Science. 15. Article 1324085. https://doi.org/10.3389/fpls.2024.1324085.
DOI: https://doi.org/10.3389/fpls.2024.1324085

Interpretive Summary: Sorghum is the fifth most important cereal crop in the world and is used as food, feed and in biofuel industry. US is the top-producer and exporter of sorghum in the world (FAO statistics). In recent years, sugarcane aphid (SCA) has emerged as serious pest in sorghum causing severe damage and significant yield loss. Although several genotypes have been identified as resistant to SCA, the genetic mechanism behind this resistance is still unclear. Thus, uncovering the resistance mechanism would be critical to aphid management. With this objective, ARS sorghum genetics team in Stillwater, OK conducted transcriptomic analysis with two sorghum genotypes, BTx623 (susceptible) and Tx2783 (resistant) in parallel. Comparative analysis between the two genotypes showed a series of genes within the genome were differentially expressed (DEGs) in response to SCA infestation and 36 DEGs were highly upregulated in the resistant line. As for their function, those defensive genes are associated sequentially with signal perception (NBS-LRR, an important resistant gene), signal transduction (MAPK signaling, salicylic acid (SA) and jasmonic acid (JA) pathways) which leads to the biosynthesis of defense compounds such as lignin, flavonoids and terpenoids. The upregulation of the 36 putative defense genes were confirmed using molecular analysis (real-time polymerase chain reaction). Furthermore, the results of phytohormone bioassay provide further evidence as application of SA and JA to the susceptible plants suppressed growth of aphid population and mitigated the damage of plants as well, suggesting their positive role in host defense against aphids. Overall, these findings shed light on the specific role of each newly identified gene in this study, thus advancing our understanding of genetic and molecular mechanisms of host plant resistance to aphids. These findings are crucial to develop sorghum crop with improved insect resistance. “The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or part of an individual's income is derived from any public assistance program. (Not all prohibited bases apply to all programs.) Persons with disabilities who require alternative means for communication of program information (Braille, large print, audiotape, etc.) should contact USDA's TARGET Center at [phone] (voice and TDD). To file a complaint of discrimination, write to USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, D.C. 20250-9410, or call [phone] (voice) or [phone] (TDD). USDA is an equal opportunity provider and employer.”

Technical Abstract: Sugarcane aphid (SCA) has emerged as a major pest of sorghum and several sorghum genotypes have shown host plant resistance to SCA. However, the molecular and genetic mechanisms underlying this resistance is still unclear. To understand these mechanisms, transcriptomic study was conducted in resistant (Tx2783) and susceptible (BTx623) sorghum genotypes infested with SCA. A principal component analysis revealed a difference in transcriptomic profiles between the two genotypes. Further, differentially expressed genes (DEGs) used for gene ontology and pathway analysis indicated the upregulation of a set of genes related to signal perception (NBS-LRR), signal transduction (MAPK signaling, salicylic acid (SA) and jasmonic acid (JA)) and defense (transcription factors, flavonoids and terpenoids). The upregulation of the selected DEGs was verified by RT-PCR analysis, which was performed with the resistant and susceptible genotypes. Further, phytohormone bioassay experiment showed a decrease in aphid population, plant mortality and damage in the susceptible genotype when treated with JA and SA. Together, those results indicated the set of genes, pathways and defense compounds were involved in host plant resistance to SCA. These findings shed light on the specific role of each DEGs; thus, advancing our understanding of genetic and molecular mechanisms of host plant resistance to aphids. USDA is an equal opportunity provider and employer.